Influenza virus mRNA trafficking through host nuclear speckles

Nature Microbiology

Volumn 1, Issue 7, 2016, Pages

  Mor, Amir ^a   White, Alexander ^a   Zhang, Ke ^a   Thompson, Matthew ^b   Esparza, Matthew ^a   Muñoz Moreno, Raquel ^c,d   Koide, Kazunori ^e   Lynch, Kristen W ^b   García Sastre, Adolfo ^c,d   Fontoura, Beatriz M A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Department of Microbiology ^*  (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INS1 PROTEIN, INFLUENZA VIRUS; M1 PROTEIN, INFLUENZA A VIRUS; M2 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN; VIRAL PROTEIN; VIRUS RNA;

ALTERNATIVE RNA SPLICING; CELL LINE; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; INFLUENZA A VIRUS; METABOLISM; PATHOGENICITY; PHYSIOLOGY; RNA SPLICING; VIROLOGY; VIRUS GENOME; VIRUS RELEASE;

ALTERNATIVE SPLICING; CELL LINE; CELL NUCLEUS; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; INTRANUCLEAR INCLUSION BODIES; RNA SPLICING; RNA, VIRAL; VIRAL MATRIX PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS RELEASE;

EID: 84988543581     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.69     Document Type: Article

References (50)

1. Spector, D. L. & Lamond, A. I. Nuclear speckles. Cold Spring Harb. Perspect. Biol. 3, a000646 (2011).
2. Mao, Y. S., Zhang, B. & Spector, D. L. Biogenesis and function of nuclear bodies. Trends Genet. 27, 295-306 (2011).
3. Saitoh, N. et al. Proteomic analysis of interchromatin granule clusters. Mol. Biol. Cell 15, 3876-3890 (2004).
4. Misteli, T., Caceres, J. F. & Spector, D. L. The dynamics of a pre-mRNA splicing factor in living cells. Nature 387, 523-527 (1997).
5. Tilgner, H. et al. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs. Genome Res. 22, 1616-1625 (2012).
6. Girard, C. et al. Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nature Commun. 3, 994 (2012).
7. Dias, A. P., Dufu, K., Lei, H. & Reed, R. A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nature Commun. 1, 97 (2010).
8. Akef, A., Zhang, H., Masuda, S. & Palazzo, A. F. Trafficking of mRNAs containing ALREX-promoting elements through nuclear speckles. Nucleus 4, 326-340 (2013).
9. Ishihama, Y., Tadakuma, H., Tani, T. & Funatsu, T. The dynamics of premRNAs and poly(A)+ RNA at speckles in living cells revealed by iFRAP studies. Exp. Cell Res. 314, 748-762 (2008).
10. Melcak, I., Melcakova, S., Kopsky, V., Vecerova, J. & Raska, I. Prespliceosomal assembly on microinjected precursor mRNA takes place in nuclear speckles. Mol. Biol. Cell 12, 393-406 (2001).
11. Dubois, J., Terrier, O. & Rosa-Calatrava, M. Influenza viruses and mRNA splicing: doing more with less. mBio 5, e00070 (2014).
12. Jackson, D. & Lamb, R. A. The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J. Gen. Virol. 89, 3097-3101 (2008).
13. Lamb, R. A., Lai, C. J. & Choppin, P. W. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc. Natl Acad. Sci. USA 78, 4170-4174 (1981).
14. Shih, S. R., Suen, P. C., Chen, Y. S. & Chang, S. C. A novel spliced transcript of influenza A/WSN/33 virus. Virus Genes 17, 179-183 (1998).
15. Wise, H. M. et al. Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathogens 8, e1002998 (2012).
16. Matera, A. G. & Wang, Z. A day in the life of the spliceosome. Nature Rev. Mol. Cell Biol. 15, 108-121 (2014).
17. Robb, N. C. & Fodor, E. The accumulation of influenza Avirus segment 7 spliced mRNAs is regulated by the NS1 protein. J. Gen. Virol. 93, 113-118 (2012).
18. Bier, K., York, A. & Fodor, E. Cellular cap-binding proteins associate with influenza virus mRNAs. J. Gen. Virol. 92, 1627-1634 (2011).
19. Wang, W. et al. Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res. 36, 4913-4928 (2008).
20. Fortes, P., Lamond, A. I. & Ortin, J. Influenza virus NS1 protein alters the subnuclear localization of cellular splicing components. J. Gen. Virol. 76(Pt 4), 1001-1007 (1995).
21. Zhang, L. et al. Inhibition of pyrimidine synthesis reverses viral virulence factormediated block of mRNA nuclear export. J. Cell Biol. 196, 315-326 (2012).
22. Wolff, T., O'Neill, R. E. & Palese, P. NS1-binding protein (NS1-BP): a novel human protein that interacts with the influenza A virus nonstructural NS1 protein is relocalized in the nucleus of infected cells. J. Virol. 72, 7170-7180 (1998).
23. Tsai, P. L. et al. Cellular RNA binding proteins NS1-BP and hnRNP K regulate influenza A virus RNA splicing. PLoS Pathogens 9, e1003460 (2013).
24. Cao, W., Razanau, A., Feng, D., Lobo, V. G. & Xie, J. Control of alternative splicing by forskolin through hnRNP K during neuronal differentiation. Nucleic Acids Res. 40, 8059-8071 (2012).
25. Marchand, V. et al. Identification of protein partners of the human immunodeficiency virus 1 tat/rev exon 3 leads to the discovery of a new HIV-1 splicing regulator, protein hnRNP K. RNA Biol. 8, 325-342 (2011).
26. Motta-Mena, L. B. et al. A disease-associated polymorphism alters splicing of the human CD45 phosphatase gene by disrupting combinatorial repression by heterogeneous nuclear ribonucleoproteins (hnRNPs). J. Biol. Chem. 286, 20043-20053 (2011).
27. Venables, J. P. et al. Multiple and specific mRNA processing targets for the major human hnRNP proteins. Mol. Cell Biol. 28, 6033-6043 (2008).
28. Sharma, A., Takata, H., Shibahara, K., Bubulya, A. & Bubulya, P. A. SON is essential for nuclear speckle organization and cell cycle progression. Mol. Biol. Cell 21, 650-663 (2010).
29. Lu, X., Ng, H. H. & Bubulya, P. A. The role of SON in splicing, development, and disease. WIREs RNA 5, 637-646 (2014).
30. Karlas, A. et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463, 818-822 (2010).
31. Hautbergue, G. M., Hung, M. L., Golovanov, A. P., Lian, L. Y. & Wilson, S. A. Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc. Natl Acad. Sci. USA 105, 5154-5159 (2008).
32. Gatfield, D. et al. The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila. Curr. Biol. 11, 1716-1721 (2001).
33. Read, E. K. & Digard, P. Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export. J. Gen. Virol. 91, 1290-1301 (2010).
34. Albert, B. J. et al. Meayamycin inhibits pre-messenger RNA splicing and exhibits picomolar activity against multidrug-resistant cells. Mol. Cancer Therapeut. 8, 2308-2318 (2009).
35. Kaida, D. et al. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nature Chem. Biol. 3, 576-583 (2007).
36. Schneider, J., Dauber, B., Melen, K., Julkunen, I. & Wolff, T. Analysis of influenza B Virus NS1 protein trafficking reveals a novel interaction with nuclear speckle domains. J. Virol. 83, 701-711 (2009).
37. Valcarcel, J., Portela, A. & Ortin, J. Regulated M1 mRNA splicing in influenza virus-infected cells. J. Gen. Virol. 72(Pt 6), 1301-1308 (1991).
38. Ilyinskii, P. O., Gabai, V. L., Sunyaev, S. R., Thoidis, G. & Shneider, A. M. Toxicity of influenza A virus matrix protein 2 for mammalian cells is associated with its intrinsic proton-channeling activity. Cell Cycle 6, 2043-2047 (2007).
39. Nayak, D. P., Balogun, R. A., Yamada, H., Zhou, Z. H. & Barman, S. Influenza virus morphogenesis and budding. Virus Res. 143, 147-161 (2009).
40. Mor, A. et al. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nature Cell Biol. 12, 543-552 (2010).
41. Cheng, H. et al. Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127, 1389-1400 (2006).
42. Luo, M. J. & Reed, R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl Acad. Sci. USA 96, 14937-14942 (1999).
43. Valencia, P., Dias, A. P. & Reed, R. Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc. Natl Acad. Sci. USA 105, 3386-3391 (2008).
44. Nemeroff, M. E., Barabino, S. M., Li, Y., Keller, W. & Krug, R. M. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′ end formation of cellular pre-mRNAs. Mol. Cell 1, 991-1000 (1998).
45. Qiu, Y. & Krug, R. M. The influenza virus NS1 protein is a poly(A)-binding protein that inhibits nuclear export of mRNAs containing poly(A). J. Virol. 68, 2425-2432 (1994).
46. Satterly, N. et al. Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc. Natl Acad. Sci. USA 104, 1853-1858 (2007).
47. Zhang, L. et al. Inhibition of pyrimidine synthesis reverses viral virulence factormediated block of mRNA nuclear export. J. Cell Biol. 196, 315-326 (2012).
48. Ayllon, J. & Garcia-Sastre, A. The NS1 protein: a multitasking virulence factor. Curr. Top. Microbiol. Immunol. 386, 73-107 (2015).
49. Kornblihtt, A. R. et al. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nature Rev. Mol. Cell Biol. 14, 153-165 (2013).
50. Valcarcel, J., Fortes, P. & Ortin, J. Splicing of influenza virus matrix protein mRNA expressed from a simian virus 40 recombinant. J. Gen. Virol. 74(Pt 7), 1317-1326 (1993).